Ancient host specificity within a single species of brood parasitic bird

Abstract

Parasites that exploit multiple hosts often experience diversifying selection for host-specific adaptations. This can result in multiple strains of host specialists coexisting within a single parasitic species. A long-standing conundrum is how such sympatric host races can be maintained within a single parasitic species in the face of interbreeding among conspecifics specializing on different hosts. Striking examples are seen in certain avian brood parasites such as cuckoos, many of which show host-specific differentiation in traits such as host egg mimicry. Exploiting a Zambian egg collection amassed over several decades and supplemented by recent fieldwork, we show that the brood parasitic Greater Honeyguide Indicator indicator exhibits host-specific differentiation in both egg size and egg shape. Genetic analysis of honeyguide eggs and chicks show that two highly divergent mitochondrial DNA lineages are associated with ground-and tree-nesting hosts, respectively, indicating perfect fidelity to two mutually exclusive sets of host species for millions of years. Despite their age and apparent adaptive diversification, however, these ancient lineages are not cryptic species; a complete lack of differentiation in nuclear genes shows that mating between individuals reared by different hosts is sufficiently frequent to prevent speciation. These results indicate that host specificity is maternally inherited, that host-specific adaptation among conspecifics can be maintained without reproductive isolation, and that host specificity can be remarkably ancient in evolutionary terms.coevolution | gentes | phylogeography | W chromosome hypothesis S pecies interactions can be powerful generators of evolutionary diversity (1, 2). In host-parasite relationships, different hosts can exert divergent selection for parasitic specialization. Although this sometimes results in speciation in the parasitic lineage (3-5), in other cases multiple strains of host specialists coexist within a single parasitic species. A textbook example is seen in avian brood parasites such as cuckoos, in which the individuals of a single parasitic species specialize on different hosts and show phenotypic differentiation in traits such as host egg mimicry (6, 7). How phenotypically distinct host races [also known as "gentes" in the context of avian brood parasitism (8)] can evolve and be maintained over evolutionary time in the face of interbreeding among conspecifics has long remained paradoxical (9-12).Genetic data have provided important insights by allowing a test of whether lineages of parasitic females consistently specialize on particular host species. Studies of the common cuckoo Cuculus canorus (13) and the shiny cowbird Molothrus bonariensis (14), both of which show host-specific phenotypic differentiation in egg traits (7, 15), have revealed subtle genetic differentiation in mitochondrial DNA (mtDNA) haplotype frequencies in relation to host use. These results are potentially consistent with the long-standing hypothesis that egg mimicry might ...

The biogeography of mitochondrial and nuclear discordance in animals

“…Interestingly, four recent studies have identified mtDNA divergence where long periods of allopatry are less likely, all of which are in avian systems. This pattern has been observed between highland and lowland mtDNA clades of the rufous-collared sparrow (Zonotrichia capensis; Cheviron & Brumfield 2009), arid and mesic clades of the karoo scrub-robin (Cercotrichas coryphaeus; Ribeiro et al 2011), eastern and western clades of the greenish warbler (Phylloscopus trochiloides; Irwin et al 2005), and between tree-nesting and ground-nesting host parasites of the greater honeyguide (Indicator indicator; Spottiswoode et al 2011). While empirical examples of such phenomena are rare, simulation studies suggest that such phylogenetic breaks can arise in the absence of barriers to gene flow if dispersal and population sizes are low (Irwin 2002) or if selection favours different mtDNA haplotypes in different environments (Irwin 2012).…”

“…Finally, a recent study of the greater honeyguide, an avian brood parasite in Africa, demonstrates strong mtDNA structure between individuals with ecologically distinct host species (ground-nesting birds versus tree nesters) with little to no structure in microsatellites (Spottiswoode et al 2011). By comparison, other taxa closely related to the greater honeyguide show much more nuclear divergence for the same mtDNA distance.…”

Supergenes and their role in evolution

“…Honeyguides have two deeply diverged mitochondrial lineages, specialising on burrow-and hole-nesting hosts (Spottiswoode et al, 2011). The available data suggest that honeyguide host races have been host-specific (ground versus tree-nesting lineages) for a long time, but that gene flow through males has prevented host races from speciating.…”

Coevolution is linked with phenotypic diversification but not speciation in avian brood parasites

“…For example, brood parasitic Vidua finches, Vidua spp., underwent sympatric speciation as they annexed novel host species [15]. Moreover, specialization on particular host species has led to genetic divergence within some cuckoo and honeyguide species into distinct host-specific races [16][17][18], and Krü ger et al [19] demonstrated that species of parasitic cuckoos had more subspecies than species of non-parasitic cuckoos. Since the appearance of these studies, novel phylogenies [20] and phylogenetic methods [3,21] have been developed.…”